In vivo microvascular structural and functional consequences of muscle length changes.

As muscles are stretched, blood flow and oxygen delivery are compromised, and consequently muscle function is impaired. We tested the hypothesis that the structural microvascular sequellae associated with muscle extension in vivo would impair capillary red blood cell hemodynamics. We developed an intravital spinotrapezius preparation that facilitated direct on-line measurement and alteration of sarcomere length simultaneously with determination of capillary geometry and red blood cell flow dynamics. The range of spinotrapezius sarcomere lengths achievable in vivo was 2.17 +/- 0.05 to 3.13 +/- 0.11 microns. Capillary tortuosity decreased systematically with increases of sarcomere length up to 2.6 microns, at which point most capillaries appeared to be highly oriented along the fiber longitudinal axis. Further increases in sarcomere length above this value reduced mean capillary diameter from 5.61 +/- 0.03 microns at 2.4-2.6 microns sarcomere length to 4.12 +/- 0.05 microns at 3.2-3.4 microns sarcomere length. Over the range of physiological sarcomere lengths, bulk blood flow (radioactive microspheres) decreased approximately 40% from 24.3 +/- 7.5 to 14.5 +/- 4.6 ml.100 g-1.min-1. The proportion of continuously perfused capillaries, i.e., those with continuous flow throughout the 60-s observation period, decreased from 95.9 +/- 0.6% at the shortest sarcomere lengths to 56.5 +/- 0.7% at the longest sarcomere lengths and was correlated significantly with the reduced capillary diameter (r = 0.711, P < 0.01; n = 18). We conclude that alterations in capillary geometry and luminal diameter consequent to increased muscle sarcomere length are associated with a reduction in mean capillary red blood cell velocity and a greater proportion of capillaries in which red blood cell flow is stopped or intermittent. Thus not only does muscle stretching reduce bulk blood (and oxygen) delivery, it also alters capillary red blood cell flow dynamics, which may further impair blood-tissue oxygen exchange.

[1]  R L Lieber,et al.  Physiologic consequences of surgical lengthening of extensor carpi radialis brevis muscle-tendon junction for tennis elbow. , 1994, The Journal of hand surgery.

[2]  S. Gray Rat spinotrapezius muscle preparation for microscopic observation of the terminal vascular bed. , 1973, Microvascular research.

[3]  A Krogh,et al.  The supply of oxygen to the tissues and the regulation of the capillary circulation , 1919, The Journal of physiology.

[4]  W. Stainsby Oxygen uptake for negative work, stretching contractions by in situ dog skeletal muscle. , 1976 .

[5]  A. Wisnes,et al.  Regional distribution of blood flow in calf muscles of rat during passive stretch and sustained contraction. , 1976, Acta physiologica Scandinavica.

[6]  C. Honig,et al.  Dual effect of oxygen on magnitude and uniformity of coronary intercapillary distance. , 1974, The American journal of physiology.

[7]  J I Hoffman,et al.  Blood flow measurements with radionuclide-labeled particles. , 1977, Progress in cardiovascular diseases.

[8]  B. Zweifach,et al.  The application of stereological principles to morphometry of the microcirculation in different tissues. , 1977, Microvascular research.

[9]  N. Banchero,et al.  Sequential perfusion of skeletal muscle capillaries. , 1985, Microvascular research.

[10]  S. Kelsen,et al.  Effect of alterations in muscle fiber length on diaphragm blood flow. , 1986, Journal of applied physiology.

[11]  G H Pollack,et al.  The cross-bridge theory. , 1983, Physiological reviews.

[12]  J. West,et al.  Capillary tortuosity in rat soleus muscle is not affected by endurance training. , 1989, The American journal of physiology.

[13]  O. Mathieu‐costello Capillary tortuosity and degree of contraction or extension of skeletal muscles. , 1987, Microvascular research.

[14]  B. Duling,et al.  A comparison of microvascular estimates of capillary blood flow with direct measurements of total striated muscle flow. , 1982, International journal of microcirculation, clinical and experimental.

[15]  B. Duling,et al.  Distribution of capillary blood flow in the microcirculation of the hamster: an in vivo study using epifluorescent microscopy. , 1984, Microvascular research.

[16]  G. Schmid-Schönbein,et al.  Effects of skeletal muscle fiber deformation on lymphatic volumes. , 1990, The American journal of physiology.

[17]  T. Musch,et al.  Skeletal muscle blood flow abnormalities in rats with a chronic myocardial infarction: rest and exercise. , 1992, The American journal of physiology.

[18]  P. Johnson,et al.  Reactive hyperemia in individual capillaries of skeletal muscle. , 1972, The American journal of physiology.

[19]  A Cutts Sarcomere length changes in muscles of the human thigh during walking. , 1989, Journal of anatomy.

[20]  D. Poole,et al.  Capillary and fiber geometry in rat diaphragm perfusion fixed in situ at different sarcomere lengths. , 1992, Journal of applied physiology.

[21]  E. Weibel,et al.  Estimating length density and quantifying anisotropy in skeletal muscle capillaries , 1983, Journal of microscopy.

[22]  J. Fridén,et al.  In vivo measurement of human wrist extensor muscle sarcomere length changes. , 1994, Journal of neurophysiology.

[23]  B. Zweifach,et al.  Micropressures and capillary filtration coefficients in single vessels of the cremaster muscle of the rat. , 1970, Microvascular research.

[24]  E. Eriksson,et al.  Microvascular dimensions and blood flow in skeletal muscle. , 1972, Acta physiologica Scandinavica.

[25]  C. Ellis,et al.  Effect of sarcomere length on total capillary length in skeletal muscle: in vivo evidence for longitudinal stretching of capillaries. , 1990, Microvascular research.

[26]  O. Hudlická,et al.  A comparison of the microcirculation in rat fast glycolytic and slow oxidative muscles at rest and during contractions. , 1987, Microvascular research.

[27]  C. Ellis,et al.  Muscle capillary-to-fiber perimeter ratio: morphometry. , 1991, The American journal of physiology.

[28]  A. Groom,et al.  Capillary diameter and geometry in cardiac and skeletal muscle studied by means of corrosion casts. , 1983, Microvascular research.

[29]  E. Weibel,et al.  Capillary tortuosity in skeletal muscles of mammals depends on muscle contraction. , 1989, Journal of applied physiology.